Skip to main content
SpringerLink
Log in

CO2 Acquisition, Concentration and Fixation in Cyanobacteria and Algae

  • Chapter
Photosynthesis

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 9))

Summary

Aquatic photosynthetic organisms face a number of unique problems with regard to the supply of CO2 for photosynthesis. These stem largely from the physical chemistry of the water phase in which they live, where the diffusion of C1 species is slow and can exists as both CO2 and HCO3− depending on the pH of the medium. Given the constraints, a number of solutions have evolved to optimize photosynthetic CO2 fixation in algae and cyanobacteria. The two chief strategies that are apparent are the development of CO2-concentrating mechanisms based on the active uptake of both CO2 and HCO3− and the evolution of more efficient forms of Rubisco which are able to fix CO2 at limiting levels of CO2. This chapter examines aspects of co-evolution of Rubisco and CO2-concentrating mechanisms in both algae and cyanobacteria. Particular emphasis is placed on what is known about the mechanism of the operation of carbon concentrating mechanisms (CCMs) in cyanobacteria and green microalgae. In cyanobacteria, multiple active C1 transporters drive the CCM on the plasma membrane. These are energized by photosynthetic ATP and NADPH production, with the NAD(P)H dehydrogenase complexes playing a critical role. A pool of HCO3− is accumulated within the cell and this is used by the Rubisco-containing carboxysome to generate CO2 within this localized micro-environment. Carboxysomal carbonic anhydrase is crucial to this CO2 generation process. For green microalgae, active C1 transport occurs at both the plasma membrane and the chloroplast envelope. A HCO3 pool is accumulated in the chloroplast stroma, with the aid of photosynthetic energy, and this pool is used to elevate CO2 around Rubisco. Rubisco is primarily localized to the pyrenoid. A crucial part of this conversion appears to be a thylakoid lumen carbonic anhydrase, which may use the lumenal protons to drive this process. The CCM is inducible in nature in both cyanobacteria and algae, increasing its affinity forexternal C1 when cells are grown at limiting C1 conditions. In both green and non-green algae, the presence of significant CCM activity is correlated with the presence of pyrenoids and single chloroplasts within cells. This chapter examines the possible diversity of CCM operation among the green and non-green algae, highlighting possible variation in CCM operations compared to the models developed for green microalgae. Considerable work remains to be done to identify specific variation of CCM mechanismsin non-green algae.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 509.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 649.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 649.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Abbreviations

CA:

carbonic anhydrase

CCM:

CO2-concentrating mechanism

C1:

inorganic carbon (CO2+HCO −3

DCMU:

dichlorodiphenylmethyl urea

PEP:

phosphoenolpyruvate

PGA:

3-phosphoglyceric acid

RuBP:

ribulose 1,5-bisphosphate

Rubisco:

ribulose bisphosphate carboxylase/oxygenase

S10:

relative specificity factor for Rubisco relating the carboxylase to oxygenase reaction kinetics (Vg*Kc/(Kc*Vo)

References

  • Adams MS (1985) Inorganic carbon reserves of natural waters and the ecophysiological consequences of their photosynthetic depletion: (II) macrophytes. In: Lucas WJ and Berry JA (eds) InorganicCarbon Uptake by Aquatic Photosynthetic Organisms, pp 421–435. American Society of Plant Physiologists, Rockville

    Google Scholar 

  • Aizawa K and Miyachi S (1984) Carbonic anhydrase located on cell surface increases the affinity for inorganic carbon in photosynthesis of Dunaliella tertiolecta. FEBS Lett 173: 41–44

    Article  CAS  Google Scholar 

  • Aizawa K and Miyachi S (1986) Carbonic-anhydrase and CO2 concentrating mechanisms in microalgae and cyanobacteria (review). FEMS Micr Rev 39: 215–233

    CAS  Google Scholar 

  • Amoroso G, Weber C, Sültemeyer DF and Fock H (1996) Intracellular carbonic anhydrase activities in Dunaliella tertiolecta (Butcher) and Chlamydomonas reinhardtii (Dangeard) in relation to inorganic carbon concentration during growth: Further evidence for the existence of two distinct carbonic anhydrases associated with the chloroplasts. Planta 199:177–184

    Article  CAS  Google Scholar 

  • Amoroso G, Sültemeyer D, Thyssen C and Fock HP (1998) Uptake of HCO3 and CO2 in cells and chloroplasts from the microalgae Chlamydomonas reinhardtii and Dunaliella tertiolecta. Plant Physiology 116: 193–201

    Article  CAS  Google Scholar 

  • Badger MR (1987) The CO2-concentrating mechanism in aquatic phototrophs. In: Hatch MD and Boardman NK (eds) The Biochemistry of Plants, Vol 10, pp 217–274. Academic Press, San Diego

    Google Scholar 

  • Badger MR and Andrews TJ (1987) Co-evolution of Rubisco and CO2 concentrating mechanisms. In: Biggins J (ed) Progress in Photosynthesis Research, Vol III, pp 601–609. Martinus Nijhoff Publishers, Dordrecht

    Google Scholar 

  • Badger MR and Price GD (1989) Carbonic anhydrase activity associated with the cyanobacterium Synechococcus PCC7942. Plant Physiol 89: 51–60

    CAS  Google Scholar 

  • Badger MR and Price GD (1992) The CO2 concentrating mechanism in cyanobacteria and microalgae. Physiol Plant 84: 606–615

    Article  CAS  Google Scholar 

  • Badger MR and Price GD (1994) The role of carbonic anhydrase in photosynthesis. Ann Rev Plant Physiol Plant Mol Biol 45: 369–392

    CAS  Google Scholar 

  • Badger MR, Kaplan A and Berry JA (1980) Internal inorganic carbon pool of Chlamydomonas reinhardtii—evidence for a carbon dioxide concentrating mechanism. Plant Physiol 66: 407–113

    CAS  Google Scholar 

  • Badger MR, Bassett M and Comins HN (1985) Amodel for HCO −3 accumulation and photosynthesis in the cyanobacterium Synechococcus sp. Theoretrial predictions and experimental observations. Plant Physiol 77: 465–471

    CAS  Google Scholar 

  • Badger MR, Palmqvist K and Yu JW (1994) Measurement of and CO2 and HCO −3 fluxes in cyanobacteria and microalgae during steady-state photosynthesis. Physiol Plant 90: 529–536

    Article  CAS  Google Scholar 

  • Badger MR, Andrews TJ, Whitney SM, Ludwig M, Yellowlees DC, Leggat W and Price GD (1998) The diversity and Coevolution of Rubisco, plastids, pyrenoids and chloroplast-based CCMs in the algae. Can J Bot 76: 1052–1071

    Article  CAS  Google Scholar 

  • Bailly J and Coleman JR (1988) Effect of CO2 concentration on protein biosynthesis and carbonic anhydrase expression in Chlamydomonas reinhardtii. Plant Physiol 87: 833–840

    CAS  Google Scholar 

  • Beardall J (1989) Photosynthesis and photorespiration in marine phytoplankton. Aquatic Botany 43: 104–130

    Google Scholar 

  • Berner RA (1990) Atmospheric carbon dioxide levels over phanerozoic time. Science 249: 1382–1386

    CAS  Google Scholar 

  • Berner RA (1993) Paleozoic atmospheric CO2 Importance of solar radiation and plant evolution. Science 261: 68–70

    CAS  Google Scholar 

  • Björk M, Haglund K, Ramazanov Z and Pedersen M (1993) Inducible mechanisms for HCO −3 utilization and repression of photorespiration in protoplasts and thalli of three species of Ulva (Chlorophyta) J Phycol 29: 166–173

    Google Scholar 

  • Bold HC and Wynne MJ (1985) Introduction to the Algae. Structure and reproduction. Prentice-Hall, Inc., Edgewood Cliffs

    Google Scholar 

  • Borodin V, Gardeström P and Samuelsson G (1994) The effect of light quality on the induction of efficient photosynthesis under low CO2 conditions in Chlamydomonas reinhardtii and Chlorella pyrenoidosa. Physiol Plant 92: 254–260

    Article  CAS  Google Scholar 

  • Broda E (1975) The Evolution of Bioenergetic Processes. Pergamon Press, Oxford

    Google Scholar 

  • Burns BD and Beardall J (1987) Utilization of inorganic carbon by marine microalgae. J Exp Mar Biol Ecol 107: 75–86

    Article  CAS  Google Scholar 

  • Burow MD, Chen Z-Y, Mouton TM and Moroney JV (1996) Isolation of cDNA clones induced upon transfer of Chlamydomonas reinhardtii cells to low CO2. Plant Mol Biol 31:443–448

    Article  CAS  PubMed  Google Scholar 

  • Chen Z-Y, Burow MD, Mason CB and Moroney JV (1996) A low-CO2-inducible gene encoding an alanine: α-ketoglutarate aminotransferase in Chlamydomonas reinhardtii. Plant Physiol 112: 677–684

    CAS  PubMed  Google Scholar 

  • Chen Z-Y, Lavigne LL, Mason CB and Moroney JV (1997) Cloning and overexpression of two cDNAs encoding the low-CO2-inducible chloroplast envelope protein LIP-36 from Chlamydomonas reinhardtii. Plant Physiol 114: 265–273

    Article  CAS  PubMed  Google Scholar 

  • Coleman JR (1991) The molecular and biochemical analyses of CO2-concentrating mechanisms in cyanobacteria and microalgae. Plant Cell Environ 14: 861–867

    CAS  Google Scholar 

  • Coleman JR and Grossman AR (1984) Biosynthesis of carbonic anhydrase in Chlamydomonas reinhardtii during adaptation to low CO2. Proc Natl Acad Sci USA 81: 6049–6053

    CAS  Google Scholar 

  • Coleman JR, Berry JA, Togasaki RK and Grossman AR (1984) Identification ofextracellular carbonic anhydrase of Chlamydomonas reinhardtii. Plant Physiol 76: 472–477

    CAS  Google Scholar 

  • Coleman JR, Luinenburg I, Majeau N and Provart N (1991) Sequence analysis and regulation of, expression of a gene coding for carbonic anhydrase in Chlamydomonas reinhardtii. Can J Bot 69: 1097–1102

    CAS  Google Scholar 

  • Delwiche CF and Palmer JD (1996) Rampant horizontal transfer and duplication of Rubisco genes in eubacteria and plastids. Mol Biol Evol 13: 873–882

    CAS  PubMed  Google Scholar 

  • Dionisio ML, Tsuzuki M and Miyachi S (1989a) Light requirement for carbonic anhydrase induction in Chlamydomonas reinhardtii. Plant Cell Physiol 30: 207–213

    CAS  Google Scholar 

  • Dionisio ML, Tsuzuki M and Miyachi S (1989b) Blue light induction of carbonic anhydrase activity in Chlamydomonas reinhardtii. Plant Cell Physiol 30: 215–219

    CAS  Google Scholar 

  • Dionisio-Sese ML, Fukuzawa H and Miyachi S (1990) Light-induced carbonic anhydrase expression in Chlamydomonas reinhardtii. Plant Physiol 94: 1103–1110

    CAS  Google Scholar 

  • Dodge J (1973) The pyrenoid. In: Dodge J (ed) The Fine Structure of Algal Cells, pp 105–124. Academic Press, London

    Google Scholar 

  • Eriksson M, Karlsson J, Ramazanov Z, Gardeström P and Samuelsson G (1996) Discovery of analgal mitochondrial carbonic anhydrase: Molecular cloning and characterization of a low-CO2-induced polypeptide in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 93: 12031–12034

    Article  CAS  PubMed  Google Scholar 

  • Eriksson M, Villand P, Gardeström P and Samuelsson G (1998) Induction and regulation of expression of a low-CO2-induced mitochondrial carbonic anhydrase in Chlamydomonas reinhardtii. Plant Physiol 116: 637–641

    Article  CAS  PubMed  Google Scholar 

  • Espie GS and Kandasamy RA (1994) Monensin inhibition of Na*-dependent HCO3 transportdistinguishes it from Na*-independent HCO3 transport and provides evidence for Na*/HCO −3 symport in the cyanobacterium Synechococcus UTEX 625. Plant Physiol 104: 1419–1428

    CAS  PubMed  Google Scholar 

  • Ettl H (1978) Xanthophyceae. In: Ettl H, Gerloff J and Heynig H (eds) Susswasserflora von Mitteleuropa. Gustav Fischer, Stuttgart

    Google Scholar 

  • Ettl H (1983) Chlorophyta I. In: Ettl H, Gerloff J and Heynig H (eds) Susswasserflora von Mitteleuropa. pp i–xiv, 1–807. Gustaff Ficher Verlag, Stuttgart

    Google Scholar 

  • Fett JP and Coleman JR (1994) Regulation of periplasmic carbonic anhydrase expression in Chlamydomonas reinhardtii by acetate and pH. Plant Physiol 106: 103–108

    CAS  PubMed  Google Scholar 

  • Fisher M, Gokhman I, Pick U and Zamir A (1996) A saltresistant plasma membrane carbonic anhydrase is induced by salt in Dunaliella salina. J Biol Chem 271: 17718–17723

    CAS  PubMed  Google Scholar 

  • Fridlyand LE (1997) Models of CO2 concentrating mechanisms in microalgae taking into account cell and chloroplast structure. Biosystems 44: 41–57

    Article  CAS  PubMed  Google Scholar 

  • Fujiwara S, Fukuzawa H, Tachiki A and Miyachi S (1990) Structure and differential expression of two genes encoding carbonic anhydrase in Chlamydomonas reinhardtii. Proc Natl Acad Sci USA 87: 9779–9783

    CAS  PubMed  Google Scholar 

  • Fukuzawa H, Fujiwara S, Yamamoto Y, Dionisio-Sese ML and Miyachi S (1990) cDNA cloning, sequence, and expression of carbonic anhydrase in Chlamydomonas reinhardtii: Regulation by environmental CO2-concentration. Proc Natl Acad Sci USA 87: 4383–4387

    CAS  PubMed  Google Scholar 

  • Fukuzawa H, Suzuki E, Komukai Y and Miyachi S (1992) A gene homologous to chloroplast carbonic anhydrase (icfA) is essential to photosynthetic carbon dioxide fixation by Synechococcus PCC7942. Proc Natl Acad Sci 89: 4437–41

    CAS  PubMed  Google Scholar 

  • Funke RP, Kovar JL and Weeks DP (1997) Intracellular carbonic anhydrase isessentialto photosynthesis in Chlamydomonas reinhardtii at atmosphericlevels of CO2. Plant Physiol 114: 237–244

    Article  CAS  PubMed  Google Scholar 

  • Garbary DJ, Hansen GI and Scagel RF (1980) Arevised classification ofthe Bangiophyceae (Rhodophyta). Nova Hedwigia 33: 145–166

    Google Scholar 

  • Garcia Sanchez MJ, Fernandez JA and Niell X (1994) Effect of inorganic carbon supply on the photosynthetic physiology of Gracilaria tenuistipitata. Planta 194: 55–61

    CAS  Google Scholar 

  • Gehl KA, Colman B, and Sposato LM (1990) Mechanism of inorganic carbon uptake in Chlorella saccharophila: The lack of involvement of carbonic anhydrase. J Exp Bot 41: 1385–1391

    CAS  Google Scholar 

  • Geraghty AM and Spalding MH (1996) Molecular and structural changes in Chlamydomonas under limiting CO2 A possible mitochondrial role in adaptation. Plant Physiol 111: 1339–1347

    CAS  PubMed  Google Scholar 

  • Geraghty AM, Anderson JC and Spalding MH (1990) A 36 kilodalton limiting-CO2 induced polypeptide of Chlamy-domonas is distinct from the 37 kilodalton periplasmic carbonic anhydrase. Plant Physiol 93: 116–121

    CAS  Google Scholar 

  • Giordano M and Maberly SC (1989) Distribution of carbonic anhydrase in British marine macroalgae. Oecologia 81: 534–539

    Article  Google Scholar 

  • Goyal A and Tolbert NE (1989) Uptake of inorganic carbon by isolated chloroplasts from air-adapted Dunaliella. Plant Physiol 89: 1264–1269

    CAS  Google Scholar 

  • Goyal A, Shiraiwa Y, Husic HD and Tolbert NE (1992) External and internal carbonic anhydrases in Dunaliella species. Marine Biol 113: 349–355

    Article  CAS  Google Scholar 

  • Griffiths DJ (1970) The pyrenoid. Bot Reviews 36: 29–58

    Google Scholar 

  • Hewett-Emmett D and Tashian RE (1996) Functional diversity, conservation, and convergence in the evolution of the α-, β-, and γ-carbonic anhydrase gene families. Mol Phylogenet Evol 5: 50–77

    CAS  PubMed  Google Scholar 

  • Higgins CT (1992) ABC transporters: From microorganisms to man. Ann Rev Cell Biol 8: 67–113

    CAS  PubMed  Google Scholar 

  • Hiltonen T, Karlsson J, Palmqvist K, Clarke AK and Samuelsson G (1995) Purification and characterisation of an intracellular carbonic anhydrase from the unicellular green alga Coccomyxa. Planta 195: 345–351

    Article  CAS  PubMed  Google Scholar 

  • Johnston AM (1991) The acquisition of inorganic carbonby marine macroalgae. Can J Bot 69: 1123–1132

    CAS  Google Scholar 

  • Johnston AM and Raven JA (1990) Effects of culture in high CO2 on the photosynthetic physiology of Fucus serratus. Br Phycol J 25: 75–82

    Google Scholar 

  • Kaneko T and Tabata S (1997) Complete genome structure of the unicellular cyanobacterium Synechocystis PCC6803. Plant Cell Physiol 38: 1171–1176

    CAS  PubMed  Google Scholar 

  • Kaplan A, Badger MR and Berry JA (1980) Photosynthesis and the intracellular inorganic carbon pool in the bluegreen alga Anabaena variabilis—response to external CO2 concentration. Planta 149: 219–226

    Article  CAS  Google Scholar 

  • Kaplan A, Zenvirth D, Marcus Y, Omata T and Ogawa T (1987) Energization and activationof inorganic carbon uptake by light in cyanobacteria. Plant Physiol 84: 210–213

    CAS  Google Scholar 

  • Kaplan A, Schwarz R, Lieman Hurwitz J and Reinhold L (1991) Physiological and molecular aspects of the inorganic carbon-concentrating mechanism in cyanobacteria. Plant Physiol 97: 851–855

    CAS  Google Scholar 

  • Kaplan A, Schwarz R, Lieman-Hurwitz J and Reinhold L (1994) Physiological and molecularstudies on the response of cyanobacteria to changes in the ambient inorganic carbon concentration. In: Bryant D (ed) The Molecular Biology of the Cyanobacteria, pp 469–485. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Karlsson J, Ramazanov Z, Hiltonen T, Garderstrüm P and Samuelsson G (1994) Effect of vanadate on photosynthesis and the ATP/ADP ratio in Low-CO2-adapted Chlamydomonas reinhardtii cells. Planta 192: 46–51

    CAS  Google Scholar 

  • Karlsson J, Hiltonen T, Husic HD, Ramazanov Z and Samuelsson G (1995) Intracellular carbonic anhydrase of Chlamydomonas reinhardtii. Plant Physiol 109: 533–539

    Article  CAS  PubMed  Google Scholar 

  • Karlsson J, Clarke AK, Chen ZY, Hugghins SY, Park YI, Husic HD, Moroney JV and Samuelsson G (1998) A novel alphatype carbonic anhydrase associated with the thylakoid membrane in Chlamydomonas reinhardtii is required for growth at ambient CO2. EMBO J 17: 1208–1216

    Article  CAS  PubMed  Google Scholar 

  • Kerby NW and Raven JA (1985) Transport and fixation of inorganic carbon by marine algae. Adv Bot Res 11: 71–123

    CAS  Google Scholar 

  • Kobayashi M, Rodriguez R, Lara C and Omata T (1997) Involvement of the C-terminal domain of an ATP-binding subunit in the regulation of the ABC-type nitrate/nitrite transporter of the cyanobacterium Synechococcus sp. strain PCC7942. J Biol Chem 272: 27197–27201

    CAS  PubMed  Google Scholar 

  • Kramer D and Findenegg GR (1978) Variations in the ultrastructure of Scenedesmus obliquus during adaptation to low CO2 level. Z Pflanzen 89: 407–410

    Google Scholar 

  • Kuchitsu K, Tsuzuki M and Miyachi S (1988a) Changes in starch localization within the chloroplast induced by changes in CO2 concentration during growth of Chlamydomonas reinhardtii: Independent regulation of pyrenoid starch and stromal starch. Plant Cell Physiol 29: 1269–1278

    CAS  Google Scholar 

  • Kuchitsu K, Tsuzuki M and Miyachi S (1988b) Characterization of the pyrenoid isolated from unicellular green alga Chlamydomonas reinhardtii: Paniculate form of RuBisCO protein. Protoplasma 144: 17–24

    Article  CAS  Google Scholar 

  • Kuchitsu K, Tsuzuki M and Miyachi S (1991) Polypeptide composition and enzyme activities of the pyrenoid and its regulation by CO2 concentration in unicellular green algae. Can J Bot 69: 1062–1069

    CAS  Google Scholar 

  • Lacoste-Royal G and Gibbs SP (1987) Immunocytochemical localization of ribulose-1,5-bisphosphate carboxylase in the pyrenoid and thylakoid region of the chloroplast of Chlamydomonas reinhardtii. Plant Physiol 83: 602–606

    CAS  Google Scholar 

  • Li QL and Canvin DT (1997) Inorganic carbon accumulation stimulates linear electron flow to artificial electron acceptors of photosystem i in air-grown cells of the cyanobacterium Synechococcus utex 625. Plant Physiol 114: 1273–1281

    CAS  PubMed  Google Scholar 

  • Lucas WJ (1983) Photosynthetic assimilation of exogenous HCO −3 by aquatic plants. Ann Rev Plant Physiol 34: 71–104

    CAS  Google Scholar 

  • Manuel LJ and Moroney JV (1988) Inorganic carbon accumulation by Chlamydomonas reinhardtii. New proteins are made during adaptation to low CO2. Plant Physiol 88: 491–496

    CAS  Google Scholar 

  • Marco E, Ohad N, Schwarz R, Lieman Hurwitz J, Gabay C and Kaplan A (1993) High CO2 concentration alleviates the block in photosynthetic electron transport in an ndhB-inactivated mutant of Synechococcus sp. PCC 7942. Plant Physiol 101: 1047–53

    Article  CAS  PubMed  Google Scholar 

  • Marek LF and Spalding MH (1991) Changes inphotorespiratory enzyme activity in response to limiting CO2 in Chlamydomonas reinhardtii. Plant Physiol 97: 420–425

    CAS  Google Scholar 

  • McKay RML and Gibbs SP (1989) Immunocytochemical localization of ribulose 1.5-bisphosphate carboxylase oxygenase in light-limited and light saturated cells of Chlorella pyrenoidosa. Protoplasma 149: 31–37

    Article  Google Scholar 

  • McKay RML and Gibbs SP (1991) Composition and function of pyrenoids: cytochemical and immunocytochemical approaches. Can J Bot 69: 1040–1052

    CAS  Google Scholar 

  • McKay RML, Gibbs SP and Espie GS (1993) Effect of dissolved inorganic carbon on the expression of carboxysomes, localization of Rubisco and the mode of inorganic carbon transport in cells of the cyanobacterium Synechococcus UTEX 625. Arch Microbiol 159: 21–29

    Article  CAS  Google Scholar 

  • Mercado JM, Niell FX and Figueroa FL (1997) Regulation of the mechanism for HCO3 use by the inorganic carbon level in Porphyra leucosticta Thur in le Jolis (rhodophyta). Planta 201: 319–325

    Article  CAS  Google Scholar 

  • Mi H, Endo T, Schreiber U, Ogawa T and Asada K (1992) Electron donation from cyclic and respiratory flows to the photosynthetic intersystem chain is mediated by pyridine nucleotide dehydrogenase in the cyanobacterium Synechocystis PCC 6803. Plant Cell Physiol 33: 1233–1237

    CAS  Google Scholar 

  • Mi H, Endo T, Schreiber U, Ogawa T and Asada K (1994) NAD(P)H dehydrogenase-dependent cyclic electron flow around photosystem I in the cyanobacterium Synechocystis PCC 6803: A study of dark-starved cells and spheroplasts. Plant Cell Physiol 35: 163–173

    CAS  Google Scholar 

  • Mi H, Endo T, Ogawa T and Asada K (1995) Thylakoid membrane-bound. NADPH-specific pyridine nucleotide dehydrogenase complex mediated cyclic electron transport in the cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol 36: 661–668

    CAS  Google Scholar 

  • Miller AG, Espie GS and Canvin DT (1990) Physiological aspects of CO2 and HCO −3 -transport by cyanobacteria: A review. Can J Bot 68: 1291–1302

    CAS  Google Scholar 

  • Miller AG, Espie GS and Canvin DT (1991) Active CO2 transport in cyanobacteria. Can J Bot 69: 925–935

    CAS  Google Scholar 

  • Miyachi S, Tsuzuki M and Avramova T (1983) Utilization modes of inorganic carbon for photosynthesis in various species of Chlorella. Plant Cell Physiol 24: 441–451

    CAS  Google Scholar 

  • Moroney JV, Husic HD and Tolbert NE (1985) Effects of carbonic anhydrase inhibitors on inorganic carbon accumulation by Chlamydomonas reinhardtii. Plant Physiol 79:177–183

    CAS  Google Scholar 

  • Moroney JV, Kitayama M, Togasaki RK and Tolbert NE (1987) Evidence for inorganic carbon transport by intact chloroplasts of Chlamydomonas reinhardtii. Plant Physiol 83: 460–463

    CAS  Google Scholar 

  • Moroney JV, Husic HD, Tolbert NE, Kitayama M, Manuel LJ and Togasaki RK (1989) Isolation and characterization of a mutant of Chlamydomonas reinhardtii deficient in the CO2 concentrating mechanism. Plant Physiol 89: 897–903

    CAS  Google Scholar 

  • Nakamura Y, Kaneko T, Hirosawa M, Miyajima N and Tabata S (1998) Cyanobase, a www database containing the complete nucleotide sequence of the genome of Synechocystis sp. strain PCC6803. Nuc Acids Res 26: 63–67

    CAS  Google Scholar 

  • Ogawa T (1990) Mutants of Synechocystis PCC6803 defective in inorganic carbon transport. Plant Physiol 94: 760–765

    CAS  Google Scholar 

  • Ogawa T (1991 a) Cloning and inactivation of a gene essential to inorganic carbon transport of Synechocystis PCC6803. Plant Physiol 96: 280–284

    CAS  Google Scholar 

  • Ogawa T (1991b) A gene homologous to the subunit-2 gene of NADH dehydrogenase is essential to inorganic carbon transport of Synechocystis PCC6803. Proc Natl Acad Sci 88: 4275–4279

    CAS  PubMed  Google Scholar 

  • Ogawa T (1992) Identification and characterization of the ictA/ ndhL gene product essential to inorganic carbon transport of Synechocystis PCC6803. Plant Physiol 99: 1604–1608

    CAS  Google Scholar 

  • Ogawa T, Miyano A and Inoue Y (1985) Photosystem-I-driven inorganic carbon transport in the cyanobacterium, Anacystis nidulans. Biochim Biophys Acta 808: 77–84

    CAS  Google Scholar 

  • Ogren WL (1984) Photorespiration—pathways, regulation, and modification. Ann Rev Plant Physiol 35: 415–442

    CAS  Google Scholar 

  • Ohkawa H, Sonoda M, Katoh H and Ogawa T (1998) The use of mutants in the analysis of the CCM in cyanobacteria. Can J Bot 76: 1035–1042

    Article  CAS  Google Scholar 

  • Okamura M, Price GD, Badger MR, Ogawa T and Omata T (1997) The cmpABCD genes of the cyanobacterium Synechococcus sp. PCC7942 encode a HCO3 transporter. Plant Cell Physiol 38: supplement: 30

    Google Scholar 

  • Omata T and Ogawa T (1985) Changes in the polypeptide composition of the cytoplasmic membrane in the cyanobacterium Anacystis nidulans during adaptation to low CO2 conditions. Plant Cell Physiol 26: 1075–1081

    CAS  Google Scholar 

  • Omata T and Ogawa T (1986) Biosynthesis of a 42-KD polypeptide in the cytoplasmic membrane of the cyanobacterium Anacystis nidulans strain-R2 during adaptation to low CO2 concentration. Plant Physiol 80: 525–530

    CAS  Google Scholar 

  • Omata T and Ogawa T (1987) Immunochemical studies on the major proteins in cytoplasmic membranes of cyanobacteria. In: Biggins J ( eds) Progress in Photosynthesis Research, Vol IV, pp 601–609. Martinus Nijhoff Publishers, Dordrecht

    Google Scholar 

  • Omata T, Andriesse X and Hirano A (1993) Identification and characterization of a gene cluster involved in nitrate transport in the cyanobacterium Synechococcus sp. PCC7942. Mol Gen Genet 236: 193–202

    Article  CAS  PubMed  Google Scholar 

  • Palmqvist K, Sundblad LG, Samuelsson G and Sundbom E (1986) A correlation between changes in luminescence decay kinetics and the appearance ofa CO2-accumulating mechanism in Scenedesmus obliquus. Photosynth Res 10: 113–123

    Article  Google Scholar 

  • Palmqvist K, Sjüberg S and Samuelsson G (1988) Induction of inorganic carbon accumulation in the unicellular green algae Scenedesmus obliquus and Chlamydomonas reinhardtii. Plant Physiol 87: 437–442

    CAS  Google Scholar 

  • Palmqvist K, Sundblad L-G, Wingsle G and Samuelsson G (1990) Acclimation of photosynthetic light reactions during induction of inorganic carbon accumulation in the green alga Chlamydomonas reinhardtii. Plant Physiol 94: 357–366

    CAS  Google Scholar 

  • Palmqvist K, Ogren E and Lernmark U (1994a) The CO2-concentrating mechanism is absent in the green alga Coccomyxa: a comparative study of photosynthetic CO2 and light responses of Coccomyxa, Chlamydomonas reinhardtii and barley protoplasts. Plant Cell Environ 17: 65–72

    CAS  Google Scholar 

  • Palmqvist K, Yu J-W and Badger MR (1994b) Carbonic anhydrase activity and inorganic carbon fluxes in low-and high-C1 cells of Chlamydomonas reinhardtii and Scenedesmus obliquus. Physiol Plant 90: 537–547

    Article  CAS  Google Scholar 

  • Palmqvist K, Sültemeyer D, Baldet P, Andrews TJ and Badger MR (1995) Characterisation of inorganic carbon fluxes, carbonic anhydrase(s) and ribulose-1,5-biphosphate carboxylase-oxygenase in the green unicellular alga Coccomyxa— Comparisons with cells low-CO2 of Chlamydomonas reinhardtii. Planta 197: 352–361

    Article  CAS  Google Scholar 

  • Pesheva I, Kodama M, Dionisio-Sese ML and Miyachi S (1994) Changes in photosynthetic characteristics induced by transferring air-grown cells of Chlorococcum littorale to high-CO2 conditions. Plant Cell Physiol 35: 379–387

    CAS  Google Scholar 

  • Pierce J, Carlson TJ and Williams JGK (1989) A cyanobacterial mutant requiring theexpression of ribulose bisphosphate carboxylase from a photosynthetic anaerobe. Proc Natl Acad Sci 86: 5753–5757

    CAS  PubMed  Google Scholar 

  • Plumed MdP, Villarejo A, RiosAdl, Garcia-Reina G and Ramazanov Z (1996) The CO2-mechanism in a starchless mutant of the green unicellular alga Chlorella pyrenoidosa. Planta 200: 28–31

    Google Scholar 

  • Price GD and Badger MR (1989a) Ethoxyzolamide inhibition of CO2 uptake in the cyanobacterium Synechococcus PCC7942 without apparent inhibition of internal carbonic anhydrase activity. Plant Physiol 89: 37–43

    CAS  Google Scholar 

  • Price GD and Badger MR (1989b) Expression of human carbonic anhydrase in the cyanobacterium Synechococcus PCC7942 creates a high CO2-tequiring phenotype. Evidence for a central role for carboxysomes in the CO2 concentrating mechanism. Plant Physiol 91: 505–513

    CAS  Google Scholar 

  • Price GD and Badger MR (1991) Evidence for the role of carboxysomes in the cyanobacterial CO2-concentrating mechanism. Can J Bot 69: 963–973

    CAS  Google Scholar 

  • Price GD, Coleman JR and Badger MR (1992) Association of carbonic anhydrase activity with carboxysomes isolated from the cyanobacterium Synechococcus PCC7942. Plant Physiol 100: 784–793

    CAS  Google Scholar 

  • Price GD, Síltemeyer D, Klughammer B, Ludwig M and Badger MR (1998) The functioning of the CO2 concentrating mechanism in several cyanobacterial strains: Areview of general physiological characteristics, genes, proteins and recent advances. Can J Bot 76: 973–1002

    Article  CAS  Google Scholar 

  • Pronina NA and Borodin VV (1993) CO2 stress and CO2 concentration mechanism: investigation by means of photosystem deficient and carbonic-anhydrase-deficient mutants of Chlamydomonas reinhardtii. Photosynthetica 28: 515–522

    CAS  Google Scholar 

  • Ramazanov Z and Cardenas J (1992) Involvement of photorespiration and glycolate pathway in carbonic anhydrase induction and inorganic carbon concentration in Chlamydomonas reinhardtii. PhysiolPlant 84: 502–508

    CAS  Google Scholar 

  • Ramazanov Z and Cardenas J (1994) Photorespiratory ammonium assimilation in chloroplasts of Chlamydomonas reinhardtii. Physiol Plant 91: 495–502

    Article  CAS  Google Scholar 

  • Ramazanov Z, Mason CB, Geraghty AM, Spalding MH and Moroney JV (1993) The low CO2-inducible 36 kD protein is localized to the chloroplast envelope of Chlamydomonas reinhardtii. Plant Physiol 101: 1195–1199

    CAS  PubMed  Google Scholar 

  • Ramazanov Z, Rawat M, Henk MC, Mason CB, Matthews SW and Moroney JV (1994) The induction of the CO2-concentrating mechanism is correlated with the formation of the starch sheath around the pyrenoid of Chlamydomonas reinhardtii. Planta 195: 210–216

    Article  CAS  Google Scholar 

  • Raven JA (1970) Exogenous inorganic carbon sourcesin plant photosynthesis. Biol Reviews 45: 167–221

    CAS  Google Scholar 

  • Raven JA (1997) CO2-concentrating mechanisms—a direct role for thylakoid lumen acidification. Plant Cell Environ 20: 147–154

    Article  CAS  Google Scholar 

  • Raven JA, Johnston AM and MacFarlane JJ (1990) Carbon metabolism. In: Cole KM and Sheath RG (eds) Biology of the Red Algae, pp 171–202. Cambridge University Press, Cambridge

    Google Scholar 

  • Raven JA, Osborne JA and Johnston AM (1985) Uptake of CO2 by aquatic vegetation. Plant Cell Environ 8: 417–425

    CAS  Google Scholar 

  • Rawat M and Moroney JV (1991) Partial characterization of a new isozyme of carboni canhydrase isolated from Chlamydomonas reinhardtii. J Biol Chem 266: 9719–9723

    CAS  PubMed  Google Scholar 

  • Rawat M and Moroney JV (1995) The regulation of carbonic anhydrase and ribulose-1,5-bisphosphate carboxylase/oxygenase activase by light and CO2 in Chlamydomonas reinhardtii. Plant Physiol 109: 937–944

    CAS  PubMed  Google Scholar 

  • Read BA and Tabita FR (1994) High substrate specificity factor ribulose bisphosphate carboxylase/oxygenase from eukaryotic marine algae and properties of recombinant cyanobacterial Rubi SCO containing ‘alga’ residue modifications. Arch Biochem Biophys 312: 210–218

    Article  CAS  PubMed  Google Scholar 

  • Reddy KJ, Masamoto K, Sherman DM and Sherman LA (1989) DNA sequence and regulation of the gene (cbpA) tencoding the 42-kilodalton cytoplasmic membrane carotenoprotein of the cyanobacterium Synechococcus sp. strain PCC 7942. J Bacteriol 171: 3486–3493

    CAS  PubMed  Google Scholar 

  • Reinhold L, Zviman M and Kaplan A (1989) A quantitative model for inorganic carbon fluxes and photosynthesis in cyanobacteria. Plant Physiol Biochem 27: 945–954

    CAS  Google Scholar 

  • Reinhold L, Kosloff R and Kaplan A (1991) Amodel for inorganic carbon fluxes and photosynthesis in cyanobacterial carboxysomes. Can J Bot 69: 984–988

    CAS  Google Scholar 

  • Roberts SB, Lane TW and Morel FMM (1997) Carbonic anhydrase in the marine diatom Thalassiosira weissflogii (bacilla-riophyceae). J Phycol 33: 845–850

    Article  CAS  Google Scholar 

  • Rolland N, Dorne AJ, Amoroso G, Síltemeyer DF, Joyard J and Rochaix JD (1997) Disruption of the plastid ycf10 open reading frame affects uptake of inorganic carbon in the chloroplast of Chlamydomonas. EMBO J 16: 6713–6726

    Article  CAS  PubMed  Google Scholar 

  • Rotatore C and Colman B (1990) Uptake of inorganic carbon by isolated chloroplasts of the unicellular green alga Chlorella ellipsoidea. Plant Physiol 93: 1597–1600

    CAS  Google Scholar 

  • Rotatore C and Colman B (1991) The acquisition and accumulation of inorganic carbon by the unicellular green alga Chlorella ellipsoidea. Plant Cell Environ 14: 377–382

    CAS  Google Scholar 

  • Rotatore C, Lew RR and Colman B (1992) Active uptake of CO2 during photosynthesis in the green alga Eremosphaera viridis is mediated by a CO2-ATPase. Planta 188: 539–545

    Article  CAS  Google Scholar 

  • Smith EC and Griffiths H (1996a) The occurrence of the chloroplast pyrenoid is correlated with the activity of a CO2-Concentrating mechanismand carbonisotope discrimination in lichens and bryophytes. Planta 198: 6–16

    Article  CAS  Google Scholar 

  • Smith EC and Griffiths H (1996b) A pyrenoid-based carbon-concentrating mechanism is present in terrestrial bryophytes of the class Anthocerotae. Planta 200: 203–212

    CAS  Google Scholar 

  • Soltes-Rak E, Mulligan ME and Coleman JR (1997) Identification and characterization of agene encodinga vertebrate-type carbonic anhydrase in cyanobacteria. J Bacteriol 179: 769–774

    CAS  PubMed  Google Scholar 

  • Spalding MH (1989) Photosynthesis and photorespiration in freshwater green algae. Aquatic Botany 34: 181–209

    Article  CAS  Google Scholar 

  • Spalding MH (1990) Effect of photon flux density on inorganic carbon accumulation and net CO2 exchange in a high-CO2-requiring mutant of Chlamydomonas reinhardtii. Photosynth Res 24: 245–252

    Article  CAS  Google Scholar 

  • Spalding MH (1998) CO2-acquisition: Acclimation to changing carbon availability. In: Rochaix J-D, Goldschmidt-Clermont M and Merchant S (eds) The Molecular Biology of Chloroplasts and Mitochondria in Chlamydomonas, pp 529–547. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  • Spalding MH and Jeffrey M (1989) Membrane-associated polypeptides induced in Chlamydomonas by limiting CO2 concentrations. Plant Physiol 89: 133–137

    CAS  Google Scholar 

  • Spalding MH and Ogren L (1982) Photosynthesis is required for inductionof the CO2-system in Chlamydomonas reinhardii. FEBS Lett 145: 41–44

    Article  CAS  Google Scholar 

  • Spalding MH and Portis AR (1985) A model of CO2 assimilation in Chlamydomonas reinhardtii. Planta 73: 268–272

    Google Scholar 

  • Spalding MH, Spreitzer RJ and Ogren WL (1983a) Carbonic anhydrase deficient mutant of Chlamydomonas requires elevated carbon dioxide concentration for photoautotrophic growth. Plant Physiol 73: 268–272

    CAS  Google Scholar 

  • Spalding MH, Spreitzer RJ and Ogren WL (1983b) Reduced inorganic carbon transport in a CO2-requiring mutant of Chlamydomonas reinhardii. Plant Physiol 73: 273–276

    CAS  Google Scholar 

  • Spalding MH, Critchley C, Govindjee and Ogren WL (1984) Influence of carbon dioxide concentration during growth on fluorescence induction characteristics of the green alga Chlamydomonas reinhardtii. Photosynth Res 5: 169–176

    Article  CAS  Google Scholar 

  • Spalding MH, Winder TL, Anderson JC, Geraghty AM and Marek LF (1991) Changes in protein and gene expression during induction of the CO2-mechanism in wildtype and mutant Chlamydomonas. Can J Bot 69: 1008–1016

    CAS  Google Scholar 

  • Spence DH and Maberly SC (1985) Occurrence and ecological importanceof HCOj useamong aquatichigher plants. In: Lucas WJ and Berry JA (eds) Inorganic Carbon Uptake by Aquatic Photosynthetic Organisms, pp. 125–144. American Society of Plant Physiologists, Rockville

    Google Scholar 

  • Spencer KG, Kimpel DL, Fisher ML, Togasaki RK and Miyachi S (1983) Carbonic anhydrase induction in Chlamydomonas reinhardtii II. Requirements for carbonic anhydrase induction. Plant Cell Physiol 24: 301–304

    CAS  Google Scholar 

  • Síltemeyer DF, Klock G, Kreutzberg K and Fock HP (1988) Photosynthesis and apparent affinity for dissolved inorganic carbon by cells and chloroplasts of Chlamydomonas reinhardtii grown at high and low CO2 concentrations. Planta 176: 256–260

    Google Scholar 

  • Síltemeyer DF, Miller AG, Espie GS, Fock HP and Canvin DT (1989) Active CO2 transport by the green alga Chlamydomonas reinhardtii. Plant Physiol 89: 1213–1219

    Google Scholar 

  • Síltemeyer DF, Fock HP and Canvin DT (1990) Mass spectrometric measurement of intracellular carbonic anhydrase activity in high and low C1 cells of Chlamydomonas. Plant Physiol 94: 1250–1257

    Google Scholar 

  • Síltemeyer D, Schmidt, C and Fock HP (1993) Carbonic anhydrases in higher plants and aquatic microorganisms. Physiol Plant 88: 179–190

    Google Scholar 

  • Síltemeyer DF, Amoroso G and Fock H (1995) Induction of intracellular carbonic anhydrases during the adaptation to low inorganic carbon concentrations in wild-type and ca-1 mutant cells of Chlamydomonas reinhardtii. Planta 196: 217–224

    Google Scholar 

  • Síltemeyer D, Klughammer B, Ludwig M, Badger MR and Price GD (1997a) Random insertional mutagenesis used in the generation of mutants of the marine cyanobacterium Synechococcussp. strain PCC7002 with animpaired CO2 concentrating mechanism. Aust J Plant Physiol 24: 317–327

    Google Scholar 

  • Síltemeyer D, Price GD, Bryant DA and Badger MR (1997b) PsaE-and ndhF-mediated electron transport affect bicarbonate transport rather than carbon dioxide uptake in the cyano-bacterium Synechococcus sp PCC7002. Planta 201: 36–42

    Google Scholar 

  • Síltemeyer D, Klughammer B, Badger MR and Price GD (1998a) Fast induction of high-affinity HCO3 transport incyanobacteria. Plant Physiol 116: 183–192

    Google Scholar 

  • Síltemeyer D, Klughammer B, Badger MR and Price GD (1998b) Protein phosphorylation and its possible involvement in the induction of the high-affinity CO2 concentrating mechanism in cyanobacteria. Can J Bot 76: 954–961

    Google Scholar 

  • Sundblad LG, Samuelsson G, Wigge B and Gardeström P (1990) Luminescence decay kinetics in relation to quenching and stimulation of dark fluorescence from high and low CO2 adapted cells of Scenedesmus obliquus and Chlamydomonas reinhardtii. Photosynth Res 23: 269–282

    Article  CAS  Google Scholar 

  • Suzuki K and Spalding MH (1989) Adaptation of Chlamydomonas reinhardtii high-CO2-requiring mutants to limiting-CO2 Plant Physiol 90: 1195–1200

    CAS  Google Scholar 

  • Talling JF (1985) Inorganic carbon reserves of natural waters and ecophysiological consequences of their photosynthetic depletion: microalgae. In: Lucas WJ and Berry JA (eds) Inorganic Carbon Uptake by Aquatic Photosynthetic Organisms, pp 403–420. American Society of Plant Physiologists, Rockville

    Google Scholar 

  • Thielmann J, Tolbert NE, Goyal A and Senger H (1990) Two systems forconcentrating CO2 and bicarbonate during photosynthesis by Scenedesmus. Plant Physiol 92: 622–629

    CAS  Google Scholar 

  • Thielmann J, Goyal A and Tolbert NE (1992) Two polypeptides in the inner chloroplast envelope of Dunaliella tertiolecta induced by low CO2 Plant Physiol 100: 2113–2115

    CAS  Google Scholar 

  • Tyrrell PN, Kandasamy RA, Crotty CM and Espie GS (1996) Ethoxyzolamide differentially inhibits CO2 uptake and Na+-independent and Na+-dependent HCO3 uptake in the cyanobacterium Synechococcus sp UTEX 625. Plant Physiol 112: 79–88

    CAS  PubMed  Google Scholar 

  • Uemura K, Anwaruzzaman, Miyachi S and Yokota A (1997) Ribulose-1,5-bisphosphate carboxylase/oxygenase from thermophilic red algae with a strong specificity for CO2 fixation. Biochem Biophys Res Comm 233: 568–571

    Article  CAS  PubMed  Google Scholar 

  • Villarejo A, Martínez F, Plumed MdP and Ramazanov Z (1996a) The induction of the CO2 concentrating mechanism in a starchless mutant of Chlamydomonas reinhardtii. Physiol Plant 98: 798–802

    Article  CAS  Google Scholar 

  • Villarejo A, Reina GG and Ramazanov Z (1996b) Regulation of the low-CO2-induclble polypeptides in Chlamydomonas reinhardtii. Planta 199: 481–485

    Article  CAS  Google Scholar 

  • Watson GMF and Tabita FR (1996) Regulation, unique gene organization, and unusual primary structure of carbon fixation genes from a marine phycoerythrin-containing cyanobacterium. Plant Mol Biol 32: 1103–1115

    Article  CAS  PubMed  Google Scholar 

  • Watson GMF and Tabita FR (1997) Microbial ribulose 1,5-bisphosphate carboxylase/oxygenase: A molecule for phylogenetic and enzymological investigation. FEMMS Microbiol Lett 146: 13–22

    CAS  Google Scholar 

  • Williams TG and Turpin DH (1987) The role of external carbonic anhydrase in inorganic carbon acquisition by Chlamydomonas reinhardtii at alkaline pH. Plant Physiol 83: 92–96

    CAS  Google Scholar 

  • Winder TL, Anderson JC and Spalding MH (1992) Translational regulation of the large and small subunits of ribulose bisphosphate carboxylase/oxygenase during induction of the CO2-mechanism in Chlamydomonas reinhardtii. Plant Physiol 98: 1409–1414

    CAS  Google Scholar 

  • Yu J-W, Price GD, Song L and Badger MR (1992) Isolation of a putativ ecarboxysomal carbonic anhydrase gene from the cyanobacterium Synechococcus PCC7942. Plant Physiol 100: 794–800

    CAS  Google Scholar 

  • Yu L, Zhao JD, Muhlenhoff U, Bryant DA and Golbeck JH (1993) PsaE is required for in vivo cyclic electron flow around PhotosystemI in the cyanobacterium Synechococcus sp. PCC7002. Plant Physiol 103: 171–180

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Molecular Plant Physiology Group, Research School of Biological Sciences, Australian National University, Canberra, 2601, ACT, Australia

    Murray R. Badger

  2. Department of Botany, Iowa State University, Ames, Iowa, 50011-1020, USA

    Martin H. Spalding

Authors
  1. Murray R. Badger
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Martin H. Spalding
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Robert Hill Institute, University of Sheffield, UK

    Richard C. Leegood

  2. Department of Botany, University of Wisconsin, USA

    Thomas D. Sharkey

  3. Research School of Biological Sciences, Australian National University, Australia

    Susanne von Caemmerer

Rights and permissions

Reprints and permissions

Copyright information

© 2000 Kluwer Academic Publishers

About this chapter

Cite this chapter

Badger, M.R., Spalding, M.H. (2000). CO2 Acquisition, Concentration and Fixation in Cyanobacteria and Algae. In: Leegood, R.C., Sharkey, T.D., von Caemmerer, S. (eds) Photosynthesis. Advances in Photosynthesis and Respiration, vol 9. Springer, Dordrecht. https://doi.org/10.1007/0-306-48137-5_16

Download citation

  • DOI: https://doi.org/10.1007/0-306-48137-5_16

  • Publisher Name: Springer, Dordrecht

  • Print ISBN: 978-0-7923-6143-5

  • Online ISBN: 978-0-306-48137-6

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation